Friday, February 06, 2009

What Causes Speciation?

The latest issue or Science magazine contains a number of articles on speciation.

The one that most interests me is Schluter (2009), a paper that discusses mechanisms of speciation. Schulter begins with ...

It took evolutionary biologists nearly 150 years, but at last we can agree with Darwin that the origin of species, "that mystery of mysteries" (1), really does occur by means of natural selection (2–5). Not all species appear to evolve by selection, but the evidence suggests that most of them do. The effort leading up to this conclusion involved many experimental and conceptual advances, including a revision of the notion of speciation itself, 80 years after publication of On the Origin of the Species, to a definition based on reproductive isolation instead of morphological differences (6, 7).

I've heard this a lot recently but it doesn't make sense to me. How could the evolution of reproductive isolation be selected?

The main question today is how does selection lead to speciation? What are the mechanisms of natural selection, what genes are affected, and how do changes at these genes yield the habitat, behavioral, mechanical, chemical, physiological, and other incompatibilities that are the reproductive barriers between new species? As a start, the many ways by which new species might arise by selection can be grouped into two broad categories: ecological speciation and mutation-order speciation. Ecological speciation refers to the evolution of reproductive isolation between populations or subsets of a single population by adaptation to different environments or ecological niches (2, 8, 9). Natural selection is divergent, acting in contrasting directions between environments, which drives the fixation of different alleles, each advantageous in one environment but not in the other. Following G. S. Mani and B. C. Clarke (10), I define mutation-order speciation as the evolution of reproductive isolation by the chance occurrence and fixation of different alleles between populations adapting to similar selection pressures. Reproductive isolation evolves because populations fix distinct mutations that would nevertheless be advantageous in both of their environments. The relative importance of these two categories of mechanism for the origin of species in nature is unknown.

Is there an expert on speciation out there who can explain this? I understand how two incipient species can adapt to different environments and become morphologically distinct but I don't understand how this kind of adaptation leads to selection for reproductive isolation. This is a problem that we discussed earlier [Testing Natural Selection: Part 2].

The second mechanism is even more difficult for me. I understand how chance mutations can arise and become fixed but to my mind this isn't natural selection. It's speciation by random genetic drift. It's just an accident that the mutations being fixed in the separated populations happen to lead to reproductive isolation.

Schluter tells us that mutation-order speciation is "distinct from genetic drift." He seems to refer to it as "selection" of some sort without explaining why. ("The unidentified component of speciation, if built by selection and not genetic drift, could be the result of either ecological or mutation-order mechanisms.") He says that the mutations that give rise to reproductive isolation are "advantageous" in both populations but they just happened to occur in one of them and not the other. Again, the question is what sort of mutations favoring reproductive isolation would be "advantageous," and therefore selected?

If the mutation arises later on in the other species will it sweep to fixation and remove the reproductive isolation barrier?

It's not clear to me that we have identified the mechanisms of reproductive isolation in a large number of examples. Schluter seems to agree,

The most obvious shortcoming of our current understanding of speciation is that the threads connecting genes and selection are still few. We have many cases of ecological selection generating reproductive isolation with little knowledge of the genetic changes that allow it. We have strong signatures of positive selection at genes for reproductive isolation without enough knowledge of the mechanisms of selection behind them. But we hardly have time to complain. So many new model systems for speciation are being developed that the filling of major gaps is imminent. By the time we reach the bicentennial of the greatest book ever written, I expect that we will have that much more to celebrate.

Given our lack of knowledge how can biologists be so confident that Darwin was right? How do they know that most speciations are due to natural selection and not random genetic drift—especially since drift and accident seem to be intuitively more likely?

Is this an example of adaptationist bias or is there really lots of evidence to support speciation by natural selection?

12 comments
:

I wouldn't consider myself an 'expert' on speciation, but let me try to approach the issue this way.

Incipient speciation, need not be driven by positive selection. Different populations of a species may fix different alleles that create pre-zygotic (i.e., behavioral) and post-zygotic (i.e., genetic) barriers to gene flow. In such a case where two populations have randomly fixed variant alleles for female preference, for example, such that said preference is detectably different in each, then cross-populations hybrids may conceivably be at a disadvantage with respect to the pure population strains. Say females prefer red in one pop, and yellow in another. Hybrid males could be orange and thus less fit - or hybrid females could have their preferences messed up, leading to reduced discrimination and thus an excess in costly matings.

Once the initial barrier is in place, selection could favor mechanisms that prevent the production of hybrids, which are very costly to females. Thus post-zygotic mechanisms can be favoured via reinforcement (see Ortiz-Barrientos et al. 2004).

There's also several models that have shown that while incipient speciation need not involve selection, directional selection could act to speed up the accumulation of things like Dobzhansky-Muller incompatibilities (anything driving protein evolution could, by chance, conceivably lead to incompatibilities when these proteins are placed in an untested genetic background).

So, while I believe that the consensus position on speciation is that it only requires drift and time, reinforcement has the potential to favour 'speciation genes' and play a major role in the process.

I've read theorizing, but no empiricism. Are there published papers that survey genetic differences between closely related species to determine, of the genetic differences between them, which show selection effects and which do not? (Is there sufficient information in any of the published chimp/human comparisons to be able to get any sort of good handle on this?) This would at least give a start on data points regarding how much genetic divergence appears to be due to selection, and how much to drift.

That question is far more difficult to answer than may be apparent! Drift is the null hypothesis against which evidence for selection is tested; thus not finding evidence of selection does not mean drift happened, only that the hypothesis of drift cannot be rejected. There are many papers that have done that for a variety of organisms (see Larracuente et al. 2008 for a recent example in fruit flies).

However, I can try to weigh in on your question by pointing out that a further complication is found in the following: Once reproductive isolation sets in, all bets are off in terms of trying to figure out whether selection was 'the' cause of speciation. Most 'speciation genes' that have been studied appear to have been subject to selection, but this is likely due to reinforcement (see above) acting on any genes that prevent the production of unfit hybrids. Incompatibilities between species will accumulate with abandon after gene flow has ceased, and any evidence of selection in such genes need not have been caused specifically by selection 'for' speciation.

However, one way that one may go about answering such a question is to see if there's more evidence for selection in very recently speciated pairs as compared to more ancient splits. This punctuational pattern would be consistent with speciation being often driven by rapid bouts of selection (either by directional selection for ecological adaptation, or reinforcement, etc.) followed by general stasis. I also happen to know a couple of people trying to get just such a study published as we speak.

I think Divalent has already tried to explain it to you, but the short answer is: sexual reproduction (gamete production, secondary sexual characters, intrasex competition, mate attraction, mating, gestation, parental care etc) is not free - in terms of energetics, time, risk of injury and disease etc. If the products of variants or species have poor fitness or are nonviable than various barriers to reproduction will be positively selected.

And before you blurt out 'Just-so stories,' why not crack the literature? There really is a research literature out there on this topic.

"The only chance elements are the initial standing variation in each population (determined by the spatio-genetic layout the population, as well as the nature of the vicariance event), and the de novo genetic variation that arises thereafter through mutation."

Indeed, but it precisely these events and no others that eventually result in any genetic incompatibility between the vicariant populations. Selection doesn't produce the variations, it simply preserves certain variations once they have arisen.

Ergo, the "engine" of genetic incompatibility (which is the underlying "engine" of speciation, according to the "modern synthesis") is not selection, but rather the random processes that produce new genetic (and presumably phenotypic) variants.

So, Larry, you are correct, and the author of the article in Science has it wrong.

Interestingly, Darwin himself made essentially the same point in the Origin of Species. In Chapter 5 ("Hybridism") he very clearly argues that selection cannot possibly result in increasing degrees of hybrid sterility. In a nutshell, sterility cannot be selected for. Darwin suggests that variations unrelated to fitness eventually accumulate and produce the reproductive incompatibility that defines species.

I've read theorizing, but no empiricism. Are there published papers that survey genetic differences between closely related species to determine, of the genetic differences between them, which show selection effects and which do not?

There are several papers on the actual mutations that give rise to reproductive incompatibility. In some cases the relevant allele appear to have been selected within one population because it is advantageous. In other cases the allele appears to have become common due to random genetic drift. [see Testing Natural Selection: Part 2 for an example of each type]

Many scientists seem to think that selection is the dominant mechanism but as far as I can tell this is mostly bias without experimental support.

And before you blurt out 'Just-so stories,' why not crack the literature? There really is a research literature out there on this topic.

I've read quite a bit about speciation and I'm quite puzzled.

A lot of the data is consistent with speciation by random genetic drift and that's why the textbooks mention it as an important possibility.

When I read papers that claim to show speciation by natural selection they often seem unconvincing. The monkey flower example that we discussed a few weeks ago is a prime example.

What puzzles me is that there are scientists who seem to be absolutely convinced that natural selection drives most speciation (reproductive isolation) when there doesn't seem to be very much solid evidence to support such a position.

I don't think many people are convinced that natural selection drives incipient speciation. There is a consensus that speciation occurs predominantly in allopatry. That excludes the presence of natural selection "for" speciation. Upon secondary contact however, many populations are reproductively isolated to some extent. The question then is: are the genetic differences due to genetic drift or natural selection?I agree with Larry that there is a bias for adaptive explanations. Well, they are more interesting :-)

How about the newly proposed hypothesis on the role of transposable elements (TEs) in speciation?

http://www.biology-direct.com/content/6/1/44

In short, TEs are likely undergo fixation in small subpopulations by genetic drift. The more active they are in a particular subpopulation, the more likely they can diverge the subpopulation and prevent it being reabsorbed into the ancestral population. The main evidence are the outbursts of new families of TEs at phylogenetic nodes.

Laurence A. Moran

Larry Moran is a Professor in the Department of Biochemistry at the University of Toronto. You can contact him by looking up his email address on the University of Toronto website.

Sandwalk

The Sandwalk is the path behind the home of Charles Darwin where he used to walk every day, thinking about science. You can see the path in the woods in the upper left-hand corner of this image.

Disclaimer

Some readers of this blog may be under the impression that my personal opinions represent the official position of Canada, the Province of Ontario, the City of Toronto, the University of Toronto, the Faculty of Medicine, or the Department of Biochemistry. All of these institutions, plus every single one of my colleagues, students, friends, and relatives, want you to know that I do not speak for them. You should also know that they don't speak for me.

Subscribe to Sandwalk

Quotations

The old argument of design in nature, as given by Paley, which formerly seemed to me to be so conclusive, fails, now that the law of natural selection has been discovered. We can no longer argue that, for instance, the beautiful hinge of a bivalve shell must have been made by an intelligent being, like the hinge of a door by man. There seems to be no more design in the variability of organic beings and in the action of natural selection, than in the course which the wind blows.Charles Darwin (c1880)Although I am fully convinced of the truth of the views given in this volume, I by no means expect to convince experienced naturalists whose minds are stocked with a multitude of facts all viewed, during a long course of years, from a point of view directly opposite to mine. It is so easy to hide our ignorance under such expressions as "plan of creation," "unity of design," etc., and to think that we give an explanation when we only restate a fact. Any one whose disposition leads him to attach more weight to unexplained difficulties than to the explanation of a certain number of facts will certainly reject the theory.

Charles Darwin (1859)Science reveals where religion conceals. Where religion purports to explain, it actually resorts to tautology. To assert that "God did it" is no more than an admission of ignorance dressed deceitfully as an explanation...

Quotations

The world is not inhabited exclusively by fools, and when a subject arouses intense interest, as this one has, something other than semantics is usually at stake.
Stephen Jay Gould (1982)
I have championed contingency, and will continue to do so, because its large realm and legitimate claims have been so poorly attended by evolutionary scientists who cannot discern the beat of this different drummer while their brains and ears remain tuned to only the sounds of general theory.
Stephen Jay Gould (2002) p.1339
The essence of Darwinism lies in its claim that natural selection creates the fit. Variation is ubiquitous and random in direction. It supplies raw material only. Natural selection directs the course of evolutionary change.
Stephen Jay Gould (1977)
Rudyard Kipling asked how the leopard got its spots, the rhino its wrinkled skin. He called his answers "just-so stories." When evolutionists try to explain form and behavior, they also tell just-so stories—and the agent is natural selection. Virtuosity in invention replaces testability as the criterion for acceptance.
Stephen Jay Gould (1980)
Since 'change of gene frequencies in populations' is the 'official' definition of evolution, randomness has transgressed Darwin's border and asserted itself as an agent of evolutionary change.
Stephen Jay Gould (1983) p.335
The first commandment for all versions of NOMA might be summarized by stating: "Thou shalt not mix the magisteria by claiming that God directly ordains important events in the history of nature by special interference knowable only through revelation and not accessible to science." In common parlance, we refer to such special interference as "miracle"—operationally defined as a unique and temporary suspension of natural law to reorder the facts of nature by divine fiat.
Stephen Jay Gould (1999) p.84

Quotations

My own view is that conclusions about the evolution of human behavior should be based on research at least as rigorous as that used in studying nonhuman animals. And if you read the animal behavior journals, you'll see that this requirement sets the bar pretty high, so that many assertions about evolutionary psychology sink without a trace.

Jerry Coyne
Why Evolution Is TrueI once made the remark that two things disappeared in 1990: one was communism, the other was biochemistry and that only one of them should be allowed to come back.

Sydney Brenner
TIBS Dec. 2000
It is naïve to think that if a species' environment changes the species must adapt or else become extinct.... Just as a changed environment need not set in motion selection for new adaptations, new adaptations may evolve in an unchanging environment if new mutations arise that are superior to any pre-existing variations

Douglas Futuyma
One of the most frightening things in the Western world, and in this country in particular, is the number of people who believe in things that are scientifically false. If someone tells me that the earth is less than 10,000 years old, in my opinion he should see a psychiatrist.

Francis Crick
There will be no difficulty in computers being adapted to biology. There will be luddites. But they will be buried.

Sydney Brenner
An atheist before Darwin could have said, following Hume: 'I have no explanation for complex biological design. All I know is that God isn't a good explanation, so we must wait and hope that somebody comes up with a better one.' I can't help feeling that such a position, though logically sound, would have left one feeling pretty unsatisfied, and that although atheism might have been logically tenable before Darwin, Darwin made it possible to be an intellectually fulfilled atheist

Richard Dawkins
Another curious aspect of the theory of evolution is that everybody thinks he understand it. I mean philosophers, social scientists, and so on. While in fact very few people understand it, actually as it stands, even as it stood when Darwin expressed it, and even less as we now may be able to understand it in biology.

Jacques Monod
The false view of evolution as a process of global optimizing has been applied literally by engineers who, taken in by a mistaken metaphor, have attempted to find globally optimal solutions to design problems by writing programs that model evolution by natural selection.